Alteration of the disulfide-coupled folding pathway of BPTI by circular permutation

Protein Science

Volumn 13, Issue 5, 2004, Pages 1182-1196

  Bulaj, Grzegorz ^a   Koehn, Rachel E ^a   Goldenberg, David P ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Bovine pancreatic trypsin inhibitor; Circular permutation; Effective concentration; Protein folding

Indexed keywords

APROTININ; DISULFIDE;

ARTICLE; BETA SHEET; CORRELATION ANALYSIS; COVALENT BOND; MATHEMATICAL COMPUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; WILD TYPE;

ANIMALS; APROTININ; CATTLE; DISULFIDES; ELECTROPHORESIS; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDES, CYCLIC; PROTEIN CONFORMATION; PROTEIN FOLDING; TRYPSIN;

BOVINAE;

EID: 1942505822     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.03563704     Document Type: Article

References (81)

1. Addlagatta, A., Krzywda, S., Czapinska, H., Otlewski, J., and Jaskölski, M. 2001. Ultrahigh-resolution structure of a BPTI mutant. Acta Crystallogr. D. 57: 649-663.
2. Beeser, S.A., Goldenberg, D.P., and Oas, T.G. 1997. Enhanced protein flexibility caused by a destabilizing amino acid replacement in BPTI. J. Mol. Biol. 269: 154-164.
3. Beeser, S.A., Oas, T.G., and Goldenberg, D.P. 1998. Determinants of backbone dynamics in native BPTI: Cooperative influence of the 14-38 disulfide and the Tyr 35 side chain. J. Mol. Biol. 284: 1581-1596.
4. Botos, I., Wu, Z., Lu, W., and Wlodawer, A. 2001. Crystal structure of a cyclic form of bovine pancreatic trypsin inhibitor. FEBS Lett. 509: 90-94.
5. Buchwalder, A., Szadkowski, H., and Kirschner, K. 1992. A fully active variant of dihydrofolate reductase with a circularly permuted sequence. Biochemistry 31: 1621-1630.
6. Buczek, O., Krowarsch, D., and Otlewski, J. 2002. Thermodynamics of single peptide bond cleavage in bovine pancreatic trypsin inhibitor (BPTI). Protein Sci. 11 924-932.
7. Bulaj, G. and Goldenberg, D.P. 1999. Early events in the disulfide-coupled folding of BPTI. Protein Sci. 8: 1825-1842.
8. -. 2001a. Mutational analysis of hydrogen bonding residues in the BPTI folding pathway. J. Mol. Biol. 313: 639-656.
9. -. 2001b. φ-Values for BPTI folding intermediates and implications for transition states. Nat. Struct. Biol. 8: 326-330.
10. 1H nuclear magnetic resonance in solution. Eur. J. Biochem. 152: 429-437.
11. Clementi, C., Jennings, P.A., and Onuchic, J.N. 2001. Prediction of folding mechanism for circular-permuted proteins. J. Mol. Biol. 311: 879-890.
12. Creighton, T.E. 1974. The single-disulphide intermediates in the refolding of reduced pancreatic trypsin inhibitor. J. Mol. Biol. 87: 603-624.
13. -. 1975. The two-disulfide intermediates and the folding pathway of reduced pancreatic trypsin inhibitor. J. Mol. Biol. 95: 167-199.
14. -. 1977. Effects of urea and guanidine-HCl on the folding and unfolding of pancreatic trypsin inhibitor. J. Mol. Biol. 113: 313-328.
15. -. 1983. An emperical approach to protein conformation, stability and flexibility. Biopolymers 22: 49-58.
16. -. 1992a. Folding pathways determined using disulfide bonds. In Protein folding (ed. T. Creighton), pp. 301-351. W.H. Freeman, New York.
17. -. 1992b. Protein folding pathways determined using disulfide bonds. BioEssays 14: 195-199.
18. Creighton, T.E. and Goldenberg, D.P. 1984. Kinetic role of a meta-stable native-like two-disulphide species in the folding transition of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 179: 497-526.
19. Dadlez, M. and Kim, P.S. 1996. Rapid formation of the native 14-38 disulfide bond in the early stages of BPTI folding. Biochemistry 35: 16153-16164.
20. Darby, N.J. and Creighton, T.E. 1993. Dissecting the disulfide-coupled folding pathway of bovine pancreatic trypsin inhibitor. Forming the first disulfide bonds in analogs of the reduced protein. J. Mol. Biol. 232: 873-896.
21. Deschrevel, B., Vincent, J.-P., Ripoll, C., and Thellier, M. 2003. Thermodynamic parameters monitoring the equilibrium shift of enzyme-catalyzed hydrolysis/synthesis reactions in favor of synthesis in mixtures of water and organic solvent. Biotechnol. Bioeng. 81: 167-177.
22. Doering, D. 1992. "Functional and structural studies of a small F-actin binding domain." Ph.D. thesis, Massachusetts Institute of Technology, Cambridge, MA.
23. Estell, D.A., Wilson, K.A., and Laskowski Jr., M. 1980. Thermodynamics and kinetics of the hydrolysis of the reactive-site peptide bond in pancreatic trypsin inhibitor (Kunitz) by Dermasterias imbricata Trypsin 1. Biochemistry 19: 131-137.
24. Fersht, A.R. 2000. Transition-state structure as a unifying basis in protein-folding mechanisms: Contact order, chain topology, stability, and the extended nucleus mechanism. Proc. Natl. Acad. Sci. 97: 1525-1529.
25. Goldenberg, D.P. 1985. Dissecting the roles of individual interactions in protein stability: Lessons from a circularized protein. J. Cell. Biochem. 29: 321-335.
26. -. 1992. Native and non-native intermediates in the BPTI folding pathway. Trends Biochem. Sci. 17: 257-261.
27. -. 1999. Finding the right fold. Nat. Struct. Biol. 6: 987-990.
28. Goldenberg, D.P. and Creighton, T.E. 1983. Circular and circularly permuted forms of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 165: 407-413.
29. -. 1984. Folding pathway of a circular form of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 179: 527-545.
30. Goldenberg, D.P., Frieden, R.W., Haack, J.A., and Morrison, T.B. 1989. Mutational analysis of a protein folding pathway. Nature 338: 127-132.
31. Grantcharova, V.P. and Baker, D. 2001. Circularization changes the folding transition state of the src SH3 domain. J. Mol. Biol. 306: 555-563.
32. Gromiha, M.M. and Selvaraj, S. 2001. Comparison between long-range interactions and contact order in determining the folding rate of two-state proteins: Application of long-range order to folding rate prediction. J. Mol. Biol. 310: 27-32.
33. Hanson, W.M., Beeser, S.A., Oas, T.G., and Goldenberg, D.P. 2003. Identification of a residue critical for maintaining the functional conformation of BPTI. J. Mol. Biol. 333: 425-441.
34. Henneke, J., Sebbel, P., and Glockshuber, R. 1999. Random circular permutation of DsbA reveals segments that are essential for protein folding and stability. J. Mol. Biol. 286: 1197-1215.
35. Homandberg, G.A., Mattis, J.A., and Laskowski Jr., M. 1978. Synthesis of peptide bonds by proteinases. Addition of organic cosolvents shifts peptide bond equilibria toward synthesis. Biochemistry 17: 5220-5227.
36. Itzhaki, L.S., Otzen, D.E., and Fersht, A.R. 1995. The structure of the transition state for folding of chymotrypsin inhibitor 2 analyzed by protein engineering methods: Evidence of a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254: 260-288.
37. Ivankov, D.N., Garbuzynskiy, S.O., Alm, E., Plaxco, K.W., Baker, D., and Finkelstein, A.V. 2003. Contact order revisited: Influence of protein size on the folding rate. Protein Sci. 12: 2057-2062.
38. Iwakura, M., Nakamura, T., Yamane, C., and Maki, K. 2000. Systematic circular permutation of an entire protein reveals essential folding elements. Nat. Struct. Biol. 7: 580-585.
39. Johnson, R.E., Adams, P., and Rupley, J.A. 1978. Thermodynamics of protein cross-links. Biochemistry 17: 1479-1484.
40. Jung, J. and Lee, B. 2001. Circularly permuted proteins in the protein structure database. Protein Sci. 10: 1881-1886.
41. Kleid, D.G., Yansura, D., Small, B., Dowbenko, D., Moore, D.M., Grubman, M.J., McKercher, P.D., Morgan, D.O., Robertson, B.H., and Bachrach, H.L. 1981. Cloned viral protein vaccine for foot-and-mouth disease: Responses in cattle and swine. Science 214: 1125-1129.
42. Li, L. and Shakhnovich, E.I. 2001. Different circular permutations produced different folding nuclei in proteins: A computational study. J. Mol. Biol. 306: 121-132.
43. Lin, T.Y. and Kim, P.S. 1989. Urea dependence of thiol-disulfide equilibria in thioredoxin: Confirmation of the linkage relationship and a sensitive assay for structure. Biochemistry 28: 5282-5287.
44. Lindberg, M.O., Tångrot, J., Otzen, D.E., Dolgikh, D.A., Finkelstein, A.V., and Oliveberg, M. 2001. Folding of circular permutants with decreased contact order: General trend balanced by protein stability. J. Mol. Biol. 314: 891-900.
45. Lindberg, M., Tångrot, J., and Oliveberg, M. 2002. Complete change of the protein folding transition state upon circular permutation. Nat. Struct. Biol. 9: 818-822.
46. Lindqvist, Y. and Schneider, G. 1997. Circular permutations of natural protein sequences: Structural evidence. Curr. Opin. Struct. Biol. 7: 422-427.
47. Luger, K., Hommel, U., Herold, M., Hofsteenge, J., and Kirschner, K. 1989. Correct folding of circularly permuted variants of a βα barrel enzyme in vivo. Science 243: 206-210.
48. Makarov, D.E. and Plaxco, K.W. 2003. The topomer search model: A simple, quantitative theory of two-state protein folding kinetics. Protein Sci. 12: 17-26.
49. Matsumura, M., Becktel, W.J., Levitt, M., and Matthews, B.W. 1989. Stabilization of phage T4 lysozyme by engineered disulfide bonds. Proc. Natl. Acad Sci. 86: 6562-6566.
50. Mendoza, J.A., Jarstfer, M.B., and Goldenberg, D.P. 1994. Effects of amino acid replacements on the reductive unfolding kinetics of pancreatic trypsin inhibitor. Biochemistry 33: 1143-1148.
51. Miller, E.J., Fischer, K.F., and Marqusee, S. 2002. Experimental evaluation of topological parameters determining protein-folding rates. Proc. Natl. Acad. Sci. 99: 10359-10363.
52. Millet, O., Loria, J.P., Kroenke, C.D., Pons, M., and Palmer III, A.G. 2000. The static magnetic field dependence of chemical exchange linebroadening defines the NMR chemical shift time scale. J. Am. Chem. Soc. 122: 2867-2877.
53. Miozzari, G.F. and Yanofsky, C. 1978. Translation of the leader region of the E. coli tryptophan operon. J. Bacteriol. 133: 1457-1466.
54. Mirny, L. and Shakhnovich, E. 2001. Protein folding theory: From lattice to all-atom models. Annu. Rev. Biophys. Biomol. Struct. 30: 361-396.
55. Mullins, L.S., Wesseling, K., Kuo, J.M., Garrett, J.B., and Raushel, F.M. 1994. Transposition of protein sequences: Circular permuation of ribonuclease T1. J. Am. Chem. Soc. 116: 5529-5533.
56. 1H NMR assignments and three-dimensional structure of Ala14/Ala38 bovine pancreatic trypsin inhibitor based on two-dimensional NMR and distance geometry. In Conformations and forces in protein folding (eds. B. Nall and K. Dill), pp. 86-114. American Association for the Advancement of Science, Washington, DC.
57. Oas, T.G. and Kim, P.S. 1988. A peptide model of a protein folding intermediate. Nature 336: 42-48.
58. Paci, E., Vendruscolo, M., Dobson, C.M., and Karplus, M. 2002. Determination of a transition state at atomic resolution from protein engineering data. J. Mol. Biol. 324: 151-163.
59. Plaxco, K.W., Simons, K.T., and Baker, D. 1998. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277: 985-994.
60. Pritchard, L. and Dufton, M.J. 1999. Evolutionary trace analysis of the Kunitz/ BPTI family of proteins: Functional divergence may have been based on conformational adjustment. J. Mol. Biol. 285: 1589-1607.
61. Schellman, J.A. 1955. Stability of hydrogen bonded peptide structures in aqueous solution. C. R. Trav. Lab. Carlsberg [Chim.] 29: 230-259.
62. 16 reactive-site peptide bond in bovine pancreatic trypsin inhibitor (Aprotinin). J. Protein Chem. 7: 633-644.
63. Sosnick, T.R., Mayne, L., and Englander, S.W. 1996. Molecular collapse: The rate-limiting step in two-state cytochrome c folding. Proteins 24: 413-426.
64. Staley, J.P. and Kim, P.S. 1994. Formation of a native-like subdomain in a partially folded intermediate of bovine pancreatic trypsin inhibitor. Protein Sci. 3: 1822-1832.
65. Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorff, J.W. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185: 60-89.
66. 15N spin relaxation times. J. Biomol. NMR 3: 141-164.
67. Uliel, S., Fliess, A., and Unger, R. 2001. Naturally occurring circular permutations in proteins. Protein Eng. 14: 533-542.
68. van den Berg, B., Chung, E.W., Robinson, C.R., Mateo, P.L., and Dobson, C.M. 1999. The oxidative refolding of hen lysozyme and its catalysis by protein disulfide isomerase. EMBO J. 18: 4794-4803.
69. Viguera, A.R., Serrano, L., and Wilmanns, M. 1996. Different folding transition states may result in the same native structure. Nat. Struct. Biol. 3: 874-880.
70. Wagner, G., Braun, W., Havel, T.F., Schaumann, T., Go, N., and Wüthrich, K. 1987a. Protein structures in solution by nuclear magnetic resonance and distance geometry: The polypeptide fold of the basic pancreatic trypsin inhibitor determined using two different algorithms, DISGEO and DISMAN. J. Mol. Biol. 196: 611-639.
71. Wagner, G., Brühwiler, D., and Wüthrich, K. 1987b. Reinvestigation of the aromatic side-chains in the basic pancreatic trypsin inhibitor by heteronuclear two-dimensional nuclear magnetic resonance. J. Mol. Biol. 196: 227-231.
72. Wedemeyer, W.J., Welker, E., Narayan, M., and Scheraga, H.A. 2000. Disulfide bonds and protein folding. Biochemistry 39: 4207-4216.
73. Weikl, T.R. and Dill, K.A. 2003. Folding kinetics of two-state proteins: Effect of circularization, permutation and crosslinks. J. Mol. Biol. 332: 953-963.
74. Weissman, J.S. and Kim, P.S. 1991. Reexamination of the folding of BPTI: Predominance of native intermediates. Science 253: 1386-1393.
75. Wlodawer, A., Deisenhofer, J., and Huber, R. 1987. Comparison of two highly refined structures of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 193: 145-156.
76. Yang, Y.R. and Schachman, H.K. 1993. Aspartate transcarbamoylase containing circularly permuted catalytic polypeptide chains. Proc. Natl. Acad Sci. 90: 11980-11984.
77. Zdanowski, K. and Dadlez, M. 1999. Stability of the residual structure in unfolded BPTI in different conditions of temperature and solvent composition measured by disulfide kinetics and double mutant cycle analysis. J. Mol. Biol. 287: 923-942.
78. Zhang, J.-X. and Goldenberg, D.P. 1997a. Mutational analysis of the BPTI folding pathway: I. Effects of aromatic → Leu substitutions on the distribution of folding intermediates. Protein Sci. 6: 1549-1562.
79. -. 1997b. Mutational analysis of the BPTI folding pathway: II. Effects of aromatic → Leu substitutions on folding kinetics and thermodynamics. Protein Sci. 6: 1563-1576.
80. Zhang, T., Bertelsen, E., Benvegnu, D., and Alber, T. 1993. Circular permutation of T4 lysozyme. Biochemistry 32: 12311-12318.
81. Zhou, H.-X. 2003. Effect of backbone cyclization on protein folding stability: Chain entropies of both the unfolded and the folded state are restricted. J. Mol. Biol. 332: 257-264.